Mobilization of theSalmonellagenomic island SGI1 and theProteusgenomic island PGI1 by the A/C2plasmid carryingblaTEM-24harboured by various clinical species of Enterobacteriaceae

Siébor, Eliane; Curraize, Claire de; Amoureux, Lucie; Neuwirth, Catherine

doi:10.1093/jac/dkw151

Cited by 27 publications

(27 citation statements)

References 17 publications

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“…They have been found so far in several Salmonella enterica serovars, Proteus mirabilis (1), and, more recently, Morganella morganii, Providencia stuartii, and Escherichia coli (2). SGI1 and its variants are inserted at the 3=-end of the chromosomal trmE (formerly thdF) gene and are mobilized specifically by IncA and IncC plasmids (1,(3)(4)(5)(6)(7). SGI1, the first variant identified, was found in Salmonella enterica serovar Typhimurium and is made up of a 27.4-kb backbone containing 28 open reading frames (ORFs) from int SGI1 (S001) to resG (S027) and S044 and a 15-kb complex class 1 integron inserted upstream of the resG gene and flanked by a 5-bp duplication (ACTTG) (8).…”

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Two New SGI1-LK Variants Found in Proteus mirabilis and Evolution of the SGI1-HKL Group of Salmonella Genomic Islands

Curraize

Siébor

Varin

et al. 2020

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Integrative mobilizable elements belonging to the SGI1-H, -K, and -L Salmonella genomic island 1 (SGI1) variant groups are distinguished by the presence of an alteration in the backbone (IS1359 replaces 2.8 kb of the backbone extending from within traN [S005] to within S009). Members of this SGI1-HKL group have been found in Salmonella enterica serovars and in Proteus mirabilis. Two novel variants from this group, designated SGI1-LK1 and SGI1-LK2, were found in the draft genomes of antibiotic-resistant P. mirabilis isolates from two French hospitals. Both variants can be derived from SGI1-PmGUE, a configuration found previously in another P. mirabilis isolate from France. SGI1-LK1 could arise via an IS26-mediated inversion in the complex class 1 integron that duplicated the IS26 element and the target site in IS6100. SGI1-LK1 also has a larger 8.59-kb backbone deletion extending from traN to within S013 and removing traG and traH. However, SGI1-LK1 was mobilized by an IncC plasmid. SGI1-LK2 can be derived from a hypothetical progenitor, SGI1-LK0, that is related to SGI1-PmGUE but lacks the aphA1 gene and one copy of IS26. The integron of SGI1-LK2 could arise via deletion of DNA adjacent to an IS26 and a deletion occurring via homologous recombination between duplicated copies of part of the integron 3=-conserved segment. SGI1-K can also be derived from SGI1-LK0. This would involve an IS26-mediated deletion and an inversion via homologous recombination of a segment between inversely oriented IS26s. Similar events can explain the configuration of the integrons in other SGI1-LK variants. IMPORTANCE Members of the SGI1-HKL subgroup of SGI1-type integrative mobilizable elements have a characteristic alteration in their backbone. They are widely distributed among multiply antibiotic-resistant Salmonella enterica serovars and Proteus mirabilis isolates. The SGI1-K type, found in the globally disseminated multiply antibiotic-resistant Salmonella enterica serovar Kentucky clone ST198 (sequence type 198), and various configurations in the original SGI1-LK group, found in other multiresistant S. enterica serovars and Proteus mirabilis isolates, have complex and highly plastic resistance regions due to the presence of IS26. However, how these complex forms arose and the relationships between them had not been analyzed. Here, a hypothetical progenitor, SGI1-LK0, that can be formed from the simpler SGI1-H is proposed, and the pathways to the formation of new variants, SGI1-LK1 and SGI1-LK2, found in P. mirabilis and other reported configurations via homologous recombination and IS26-mediated events are proposed. This led to a better understanding of the evolution of the SGI1-HKL group.

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Two New SGI1-LK Variants Found in Proteus mirabilis and Evolution of the SGI1-HKL Group of Salmonella Genomic Islands

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Siébor

Varin

et al. 2020

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“…[24] showed SGI1 mobilization when the IncC helper plasmid resides in the recipient strain. Since SGI1 is not self-transmissible, this observation suggests that prior to SGI1 mobilization, the donor strain acquires the IncC plasmid, which can then mobilize SGI1 toward the recipient.…”

Section: Resultsmentioning

confidence: 99%

Salmonella genomic island 1 (SGI1) reshapes the mating apparatus of IncC conjugative plasmids to promote self-propagation

et al. 2017

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IncC conjugative plasmids and Salmonella genomic island 1 (SGI1) and relatives are frequently associated with multidrug resistance of clinical isolates of pathogenic Enterobacteriaceae. SGI1 is specifically mobilized in trans by IncA and IncC plasmids (commonly referred to as A/C plasmids) following its excision from the chromosome, an event triggered by the transcriptional activator complex AcaCD encoded by these helper plasmids. Although SGI1 is not self-transmissible, it carries three genes, traNS, traHS and traGS, coding for distant homologs of the predicted mating pore subunits TraNC, TraHC and TraGC, respectively, encoded by A/C plasmids. Here we investigated the regulation of traNS and traHGS and the role of these three genes in the transmissibility of SGI1. Transcriptional fusion of the promoter sequences of traNS and traHGS to the reporter gene lacZ confirmed that expression of these genes is inducible by AcaCD. Mating experiments using combinations of deletion mutants of SGI1 and the helper IncC plasmid pVCR94 revealed complex interactions between these two mobile genetic elements. Whereas traNC and traHGC are essential for IncC plasmid transfer, SGI1 could rescue null mutants of each individual gene revealing that TraNS, TraHS and TraGS are functional proteins. Complementation assays of individual traC and traS mutants showed that not only do TraNS/HS/GS replace TraNC/HC/GC in the mating pore encoded by IncC plasmids but also that traGS and traHS are both required for SGI1 optimal transfer. In fact, remodeling of the IncC-encoded mating pore by SGI1 was found to be essential to enhance transfer rate of SGI1 over the helper plasmid. Furthermore, traGS was found to be crucial to allow DNA transfer between cells bearing IncC helper plasmids, thereby suggesting that by remodeling the mating pore SGI1 disables an IncC-encoded entry exclusion mechanism. Hence traS genes facilitate the invasion by SGI1 of cell populations bearing IncC plasmids.

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“…mirabilis.) The same sequence of the attB site as that of the SGI1-W attP site in PsTAN3 was detected in the IncA/C2-bla TEM-24 -carrying P. stuartii strain 719, which was used as an experimental recipient for SGI1 mobilization (8). The left and right junctions of SGI1-W have been amplified using primers PstLJ1(ϩ) (5=-GCACTTAGCTC AAGGTCATGA-3=)/LJ-R1 (5=-AGTTCTAAAGGTTCGTAGTCG-3=) and 104RJ (ϩ) (5=-CTGACGAG CTGAAGCGAATTG-3=)/Transf-Pstuartii-outR (5=-TTGTGCATTCGGCTCTTC-3=), respectively (SGI1-W left junction GenBank accession no.…”

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“…The left and right junctions of SGI1-W have been amplified using primers PstLJ1(ϩ) (5=-GCACTTAGCTC AAGGTCATGA-3=)/LJ-R1 (5=-AGTTCTAAAGGTTCGTAGTCG-3=) and 104RJ (ϩ) (5=-CTGACGAG CTGAAGCGAATTG-3=)/Transf-Pstuartii-outR (5=-TTGTGCATTCGGCTCTTC-3=), respectively (SGI1-W left junction GenBank accession no. LC411942) (2,6,8).…”

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Emergence of Salmonella Genomic Island 1 Variant SGI1-W in a Clinical Isolate of Providencia stuartii from Egypt

Soliman

Nariya

Shimamoto

2019

Antimicrob Agents Chemother

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M ost of the variants of Salmonella genomic island 1 (SGI1) are multidrug resistance (MDR) DNA elements that can be transferred by horizontal gene transfer (HGT) (1). SGI1 was initially described in Salmonella enterica serovar Typhimurium DT104 (1). It consists of a 27.4-kb backbone (28 open reading frames [ORFs]) with an MDR region consisting of a 15-kb complex class 1 integron of the family In104 (1). The SGI1 variant SGI1-L was detected for the first time in Proteus mirabilis and Morganella morganii strains from Palestine in 2006 and from France in 2017, respectively (2, 3). The 3= end of the chromosomal trmE gene is the SGI1-specific integration site in the SGI1-carrying strains (3, 4). Providencia stuartii is Gram-negative bacterium of the family Morganellaceae commonly associated with urinary tract infections or indwelling urinary catheters in hospitalized and nursing home patients (5). It has intrinsic resistance to polymyxin, tigecycline, aminopenicillin, and first-generation cephalosporins (5). Here, we report the first identification (to our knowledge) of SGI1 in a multidrugresistant clinical isolate of P. stuartii. The strain, designed PsTAN3, was isolated from a wound pus swab from a male patient in a teaching hospital in Tanta City, Egypt, in 2014. PsTAN3 was resistant to aztreonam (MIC, Ն512 g/ml), ciprofloxacin (MIC, Ն16 g/ml), chloramphenicol (MIC, Ն512 g/ml), colistin (MIC, Ն128 g/ml), gentamicin (MIC, Ն128 g/ml), tetracycline (MIC, Ն128 g/ml), streptomycin (MIC, Ն512 g/ml), cefoxitin (MIC, Ն256 g/ml), cefoperazone (MIC, Ն512 g/ml), trimethoprim (MIC, Ն512 g/ml), cefotaxime (MIC, Ն512 g/ml), meropenem (MIC, Ն16 g/ml), and nalidixic acid (MIC, Ն512 g/ml) but sensitive to doripenem (MIC, Յ1 g/ml). PsTAN3 was negative by the modified carbapenem inactivation method (mCIM), indicating the absence of carbapenemase production. PCR and DNA sequencing were used to map the entire SGI1 (for a list of PCR primers, see Table S1 in the supplemental material) and identified variant SGI1-W (6, 7). The multidrug resistance region was 6.54 kb with the genetic arrangement intI1-aadA2-lnuF-qacE⌬1-sul1-orf5-orf6-IS6100 (PsTAN3 class 1 integron GenBank accession no. LC370342) (Fig. 1). SGI1-W was integrated at the 3= end of the trmE gene (Fig. 1). The strain also carried bla TEM-1 , bla DHA-1 , qnrD, and floR genes conferring resistance to third-generation cephalosporins, ciprofloxacin, florfenicol, and chloramphenicol, respectively, and the class 1 integrons aadA2 and lnuF. The MDR region of SGI1 in PsTAN3 was 100% identical to that of SGI1-PmC105 reported in a P. mirabilis isolate from a poultry farm in China (7). Furthermore, the circular form was detected in PsTAN3 after two steps of DNA amplification using primers SGI1circ1 and SGI1circ2 with the expected target size (364 bp) (GenBank accession no. LC370343) (see Fig. S1A in the supplemental material). The sequence of the SGI1-W attP site in PsTAN3 (5=-TTCTGTATCGGGAAGTAA-3=) differs in 1 bp (C¡T) from that of S. enterica DT104 and P. mirabilis (5=-TTCTGTATTGGGAAG...

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Mobilization of theSalmonellagenomic island SGI1 and theProteusgenomic island PGI1 by the A/C₂plasmid carryingbla_TEM-24harboured by various clinical species of Enterobacteriaceae

Abstract: This is the first known description of SGI1 mobilization into a broad range of enterobacterial species harbouring an A/C2 plasmid and the first demonstration of PGI1 movement. The A/C2 plasmid is responsible for the GI mobilization.

Cited by 27 publications

References 17 publications

Two New SGI1-LK Variants Found in Proteus mirabilis and Evolution of the SGI1-HKL Group of Salmonella Genomic Islands

Two New SGI1-LK Variants Found in Proteus mirabilis and Evolution of the SGI1-HKL Group of Salmonella Genomic Islands

Salmonella genomic island 1 (SGI1) reshapes the mating apparatus of IncC conjugative plasmids to promote self-propagation

Emergence of Salmonella Genomic Island 1 Variant SGI1-W in a Clinical Isolate of Providencia stuartii from Egypt

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